1. Historical versus Current Distribution. Introduced in the United States. African clawed frogs (Xenopuslaevis) were used widely during the 1940s and 1950s as laboratory animals for human pregnancy testing. Animals that were released or had escaped from laboratory stocks, and from the pet trade are the sources of introduced populations. Clawed frogs are still popular in the pet trade in many states. However, concern over the potential impacts of introductions has led to banning their possession in Arizona, California, Florida, Louisiana, Nevada, and Utah (St. Amant et al., 1973; Badger and Netherton, 1995; Tinsley and McCoid, 1996).

Feral clawed frogs have been found in Colorado, Florida, Nevada, New Mexico, North Carolina, Texas, Utah, Virginia, Wisconsin, and Wyoming (Mardht and Knefler, 1973; Bacchus et al., 1993; Tinsley and McCoid, 1996; Blair et al., 1997), but have not established reproducing populations that have persisted over time. Arizona and California are the only states in which apparently permanent populations are known. Other extralimital populations have been documented in Great Britain, the Netherlands, Chile, and Ascension Island (Loveridge, 1959; Veloso and Navarro, 1988; Tinsley and McCoid, 1996).

Most authorities believe that the introduced populations of African clawed frogs found around the world are the subspecies Xenopusl. laevis, descendants of animals originally collected from native populations in South Africa (Carr et al., 1987; Tinsley and McCoid, 1996). There has been speculation that > 1 taxon may be established in California (Stebbins, 1985; M.R. Jennings, 1987a), which has not been confirmed by molecular-level investigations (Carr et al., 1987). All specimens examined from California populations have been morphologically identical to X. l. laevis. In addition, only females of X. l. laevis attain sizes greater than 100 mm in Africa (Kobel et al., 1996), and all long-established populations in California produce individuals larger than this.

Reproduction by feral clawed frogs has been documented in five states: Arizona, California, North Carolina, Virginia, and Wisconsin. The North Carolina and Wisconsin frogs have not persisted, largely due to winter temperature extremes (Tinsley and McCoid, 1996). The Virginia population, first noted in 1982 at the Gulf Branch Nature Center, Arlington, (Zell, 1986), was extirpated by the late 1980s (Tinsley and McCoid, 1996). The Arizona population was introduced in the 1960s to artificial bodies of water on the Arthur Pack Golf Course in Tucson and has remained confined to these sites (Tinsley and McCoid, 1996).

First found as a feral animal in California in 1968 (St. Amant and Hoover, 1969), clawed frogs have since become established in many Southern California drainages, including sites in Los Angeles, Orange, Riverside, San Bernardino, San Diego, Santa Barbara, and Ventura counties (McCoid and Fritts, 1980b; Lafferty and Page, 1997; S. Sweet, personal communication; D. Holland, personal communication). Citations listing clawed frogs in Imperial County (Mardht and Knefler, 1972; Stebbins, 1985) have never been substantiated. The discovery of disjunct populations in California is summarized in Table 8. The details surrounding the collection and reporting of almost all of these populations indicate that frogs were present for some period of time prior to their discovery, in some cases probably as long as several years.

The initial establishment of these widely separated, discontinuous populations was clearly the result of separate introduction events. Today, 25–30 yr after the initial discovery of these populations, clawed frogs have now spread throughout most of the drainages that contained the original release sites. For example, populations in Orange County have spread from the coastal plain in the north to the San Diego Creek and Upper Newport Bay drainages and the foothills of the Santa Ana Mountains as far south as Aliso Creek (B. Goodman, personal communication). In Orange County, clawed frogs have also spread throughout the Santa Ana River drainage into western Riverside and San Bernardino counties (B. Goodman, personal communication).

Clawed frogs originally discovered in tributaries of the Santa Clara River (Zacuto, 1975) have invaded the river and colonized both upstream (J. Dole, personal communication) and downstream to the river's mouth (Lafferty and Page, 1997), now inhabiting the tributaries in Agua Dulce, Soledad, Placerita, and San Francisquito canyons (Tinsley and McCoid, 1996; S. Bautista, personal communication). The clawed frogs first noted in Lake Munz have now colonized neighboring Hughes Lake and Elizabeth Lake and are found throughout the Leona Valley in Amargosa Creek and its tributaries (personal observations). In San Diego County, the Sweetwater, Otay, and Tijuana rivers are now colonized by clawed frogs (R. Fisher, personal communication). These patterns of dispersal mimic patterns of clawed frog dispersal in Africa, where frogs in rivers are carried downstream from breeding habitats, actively move upstream toward headwaters, and utilize human-created bodies of water as "stepping stones" to invade new habitats (van Dijk, 1977).

Some clawed frog populations have stayed confined to relatively discrete locations. The Goleta Slough and Edwards Air Force Base populations have not expanded (the latter primarily due to lack of suitable nearby habitat), and > 20 yr after their discovery, clawed frogs from Vail Lake have not moved downstream to invade the main part of the Santa Margarita River drainage (R. Fisher, personal communication).

Clawed frogs are intolerant of water loss (Hillman, 1980) and not capable of sustained overland travel through the xeric habitats of Southern California. In some areas, the sheer distance between suitable aquatic habitats may thus present an insurmountable barrier to invasion. Most of the spread of the species between drainages has likely been the result of human intervention.

Thirty years after their introduction to California, some patterns of distribution and dispersal of clawed frogs emerge: (1) populations are derived from independent introduction events in five of the counties they now inhabit (San Bernardino and Ventura counties were colonized from neighboring counties); (2) lotic (flowing water) systems are susceptible to complete colonization, including into their brackish interface with tidal waters (e.g., Santa Clara and Sweetwater rivers); (3) some climatic and biological barriers seem to prevent or retard their spread (discussed below); clawed frogs are not present in all apparently suitable habitats (e.g., Santa Barbara and Southern Riverside counties); (4) desert wetlands can sustain clawed frog populations (e.g., Piute Ponds on Edwards Air Force Base); (5) if human-aided introductions continue, there are few freshwater aquatic habitats in California that are not at risk for colonization. Waters that flow either rapidly all year or freeze over completely are among the few systems likely to remain free from invasion.

2. Historical versus Current Abundance. Although clawed frogs can avoid and survive dry conditions, drought can inhibit both breeding and recruitment, and drought has probably retarded its spread in parts of Southern California. McCoid et al. (1993) recorded declines in populations at some California sites after the extended drought from 1987–'91.

The introduction of the largemouth bass (Micropterussalmoides) has been implicated in the decline of clawed frogs in Africa, where these frogs are a popular fish bait (Hey, 1949; Mardht and Knefler, 1973). In Southern California, observers believe that the presence of fish has limited the expansion and/or population levels of clawed frogs (Zacuto, 1975; McCoid and Fritts, 1980a).

Introduced animals, including anurans, when released from the limiting effects of predation and interspecific competition, may reach higher densities at colonized sites than where they are indigenous (for anurans see Cohen and Howard, 1958; Lampo and Bayliss, 1996; Lampo and De Leo, 1998). At some sites clawed frogs exist in truly remarkable densities, for example in African fish-free lakes (Tinsley et al., 1996) as aquaculture pests (Schoonbee et al., 1979; Hepher and Pruginin, 1981; Prinsloo et al., 1981; Schramm, 1986), and in California sites free from predatory fish, where their numbers expand to fill the trophic levels fish would normally occupy (Crayon and Hothem, 1998). For example, visual surveys of surfacing frogs, combined with sampling by seining, produced a population estimate of at least 150,000 frogs at Piute Ponds on Edwards Air Force Base, Los Angeles County (unpublished data).

Efforts to eradicate clawed frogs in California are not usually successful (St. Amant, 1975; Zacuto, 1975). There is one known case in which a population in California was permanently eradicated by human efforts—the population on the University of California, Davis campus, Yolo County, cited above. The colonized habitat was a constructed, discrete body of water, which limited frogs to an area where they could be poisoned effectively.

Adult clawed frogs left the water during unsuccessful attempts to poison using rotenone at Vasquez Rock, the site of one of the first populations detected in the upper Santa Clara River drainage (St. Amant, 1975; Zacuto, 1975). Subsequent attempts to develop effective protocols for poisoning in the Santa Clara River also were unsuccessful (J. Dole, personal communication).

Other strategies for removal of clawed frogs include draining all the water from ponds, collecting frogs by seine or trap, electroshocking (Zacuto, 1975; Branning, 1979), and introducing predatory fish (Prinsloo et al., 1981). Early suggestions of biological control (i.e., introducing spiny softshell turtles [Trionyxspiniferus; Zacuto, 1975] and American alligators [Alligatormississippiensis; Mardht and Knefler, 1973]) wisely were never implemented.

None of these eradication methods have been proven capable of removing all frogs from a habitat or preventing their reintroduction from nearby unaffected areas. The extirpations of clawed frogs from sites in North Carolina, Wisconsin, and Virginia were apparently aided by sub-freezing winter temperatures (Tinsley and McCoid, 1996).

Larvicides are often used to remove anuran larvae when they become pests to aquaculture operations (Helms, 1967; Carmichael, 1983; Kane and Johnson, 1989; Theron et al., 1992; Gabbadon and Chapman, 1996), however, they have not been used against clawed frog larvae in nature.

3. Life History Features.

A. Breeding.

i. Breeding migrations. In Africa, clawed frogs are known to migrate to newly filled seasonal rainpools for breeding (Hey, 1949; Thurston, 1967; Balinsky, 1969; Mardht and Knefler, 1973). Feral clawed frogs in Wales migrated 0.2 km in late spring to a spawning site (Tinsley and McCoid, 1996). Such migrations have not been observed in U.S. populations.

Reproduction occurs any time from January–November in California, but is usually confined to late spring, between March and June (McCoid and Fritts, 1989). Male calling intensity peaks in April–May (McCoid, 1985). Patterns of reproduction in Arizona populations have not been examined.

ii. Breeding habitat. Same as adult habitat.

B. Eggs.

i. Egg deposition sites. Eggs are deposited singly or a few at a time on aquatic plants, rocks, and other benthic structures.

ii. Clutch size. In California, females exhibit asynchronous breeding periods and multiple ovipositions in a single season, depositing hundreds to several thousand eggs at a time; a large female may contain up to 17,000 ova (McCoid and Fritts, 1995). Larvae hatch within 2–3 d (Bles, 1905). Eggs and newly hatched larvae of clawed frogs and western toads (Bufoboreas) can often co-occur at sites (personal observations).

b. Cover. Larvae are free-swimming within 1–2 d after hatching (stage 47; McCoid and Fritts, 1980a). Because they are weak swimmers (Hoff and Wassersug, 1986), larvae are especially vulnerable to fish predation, and they school in the middle of deeper water to feed, rather than hiding in shallows (Wassersug and Hessler, 1971).

iii. Larval polymorphisms. None reported.

iv. Features of metamorphosis. Developmental stages were described in detail by Nieuwkoop and Faber (1994).

v. Post-metamorphic migrations. Recently metamorphosed clawed frogs migrated overland to colonize a site 0.8 km from their natal pond in Riverside County. Metamorphic animals were also observed migrating overland during a rain in San Diego County, using sheet flooding to facilitate movement (McCoid and Fritts, 1980b).

D. Juvenile Habitat. Not known to be different from adult habitat.

E. Adult Habitat. In extralimital populations, clawed frogs have repeatedly shown plasticity in habitat characteristics such as food availability, vegetation, substrate, turbidity, salinity, water temperature, and hydrology. This makes a precise characterization of habitat characteristics difficult. Highest densities of frogs are reached in permanent, eutrophic, fish-free waters that have soft substrates and submerged vegetation, and do not freeze over but remain above 20 ˚C for most of the year. Southern California's milder climate (relative to South Africa) seems to accelerate larval development, expand the breeding period, and result in greater adult growth and fat deposition (McCoid and Fritts, 1993, 1995).

Many introduced clawed frog populations are in disturbed or human-made bodies of water (McCoid and Fritts, 1993), such as drainage ditches, flood control channels, golf course ponds, manmade lakes, irrigation canals, cattle tanks, and sewage plant effluent ponds. This affinity for opportunistic colonizing of disturbed habitats is also seen in the parts of Africa where the species' range is expanding. Human-made irrigation canals, lakes, and ponds are especially favored habitats there (Picker, 1985; van Dijk, 1997; Curtis et al., 1998).

F. Home Range Size. Mark-recapture data for two populations in South Wales revealed that distances individuals traveled between captures were under 100 m at one location and 0.2–2 km at another (Measey and Tinsley, 1998).

G. Territories. Group feeding and the swarming of individuals to baited traps suggests that territories are not strictly maintained, if present. Densities can be extremely variable in response to seasonal changes in the extent of the aquatic habitat. Densities greater than 1/m2 can be achieved when populations are compressed in drying habitats in California (unpublished data).

H. Aestivation/Avoiding Dessication. Clawed frogs address the problems of increasing temperatures and decreasing water depth in summer in a number of different ways. In Southern California, individuals construct pits 30–40 cm deep in the mud of evaporating ponds, wherein water remains around 10 ˚C below the surface temperature of the water (McCoid and Fritts, 1980b). In arid parts of South Africa where ponds dry up seasonally, clawed frogs often burrow deep into the mud to outlast a dry period (Wager, 1965; Balinsky et al., 1967). They are capable of surviving at least 8 mo of starvation in this state (Hewitt and Power, 1913). Clawed frogs also alter the osmotic concentration of body fluids by the retention of urea and, in this hypertonic state, minimize water loss to the surrounding substrate (Balinsky et al., 1967; Stebbins and Cohen, 1995). This ability, coincidentally, makes them one of the most tolerant frogs to saltwater, and predisposes them to invading brackish habitats (Munsey, 1972; Romspert, 1976).

I. Seasonal Migrations. Xenopus species in Africa occasionally undertake mass migrations to other water sources when ponds dry up (Hewitt and Power, 1913; Hey, 1949; Loveridge, 1953). Similar behavior was observed during the draining of the San Joachin Reservoir in Newport Beach, California, in 1984. At some critically low water level, a resident population of clawed frogs migrated en masse from the reservoir in a single night and were seen traveling over nearby roads (B. Taylor and D. Otsuka, personal communication). This reservoir had a solid asphalt bottom that precluded frogs from digging down to avoid desiccation and probably precipitated their exodus.

J. Torpor (Hibernation). Poorly documented. Surfacing activity is greatly diminished during colder months in California populations. Nevertheless, frogs in water bodies that ice up at the edges during the winter remain active enough to come to baited traps (unpublished data). Frogs in the extirpated Virginia populations were also sampled by trapping when the pond’s surface was frozen (McCoid and Fritts, 1995).

K. Interspecific Associations/Exclusions. In California, clawed frogs are sympatric with western toads, red-spotted toads (B. punctatus), California red-legged frogs (Ranadraytonii), introduced American bullfrogs (R. catesbeiana), Pacific treefrogs (Pseudacrisregilla), and western spadefoot toads (Speahammondii). Concern over the impacts on these native anurans is not unreasonable; clawed frogs are known to eat Rana and Bufo larvae in Africa (Schramm, 1986). Under confined conditions, such as in aquaria, clawed frogs readily consume larvae of California's anurans (Bufo, Rana, and Hyla; Lenaker, 1972).

The strongest evidence of negative interactions is for western toads. Clawed frogs have been documented eating both larval and recent metamorphic western toads (Lenaker, 1972). In a sample of 39 adult clawed frogs collected from the Amargosa Creek drainage by David Muth in June 1998, the stomachs of 4 frogs contained 10 small (1.5–2.0 cm SVL) western toads. Because clawed frogs have also invaded the habitats of Pacific treefrogs (Lenaker, 1972; Mardht and Knefler, 1972), red-spotted toads (Crayon, 1997), and western spadefoot toads (E. Ervin, personal communication), there is no reason to expect these species would be exempt from predation.

Early accounts of clawed frogs in California claimed that they were eating bullfrog tadpoles and were responsible for eliminating California red-legged frogs from certain sites (Branson, 1975; Zacuto, 1975). These claims have not been substantiated. California red-legged frogs are virtually extirpated from Southern California south of the Santa Clara River, including from areas that clawed frogs have not invaded. The causes of California red-legged frog declines are the subject of some debate, and are likely symptomatic of a suite of problems (Moyle, 1973; Hayes and Jennings, 1986). Clawed frogs are sympatric with California red-legged frogs at a site in northern Los Angeles County (K. Swaim, unpublished data), but their interactions remain unexamined.

Where thorough systematic surveys were conducted for herpetofauna in Southern California, clawed frogs and American bullfrogs were not found to co-occur frequently (R. Fisher, unpublished data). It is unknown whether this is due to exclusion by competition or predation or due to divergent habitat preferences.

In African populations, the average size of adult females is 110 mm SVL (maximum 130 mm SVL); males are 3/4 as large (Kobel et al., 1996). Adults attain a larger maximum size in California populations. Two females collected on Edwards Air Force Base exceeded 140 mm SVL, which is larger than published records for the species in Africa. Early size records in California were likely from populations that were not yet fully mature. If extralimital clawed frogs reach a maximum age ≥ 16 yr, recorded for frogs in South Wales (Measey and Tinsley, 1998), then populations in California may not have contained the oldest and largest size classes before the mid 1980s.

N. Feeding Behavior. Adults are primarily aquatic consumers of slow-moving invertebrates; they are often characterized as rather inept at capturing actively swimming prey (Avila and Frye, 1978; however see Lafferty and Page, 1997). They rely upon olfaction and the lateral line system retained after metamorphosis to detect waterborne scents and the movements of aquatic prey; they can even find food and feed when blinded (Elepfandt, 1996).

A passage from Tinsley et al. (1996, p. 44) concerning feeding ability is illuminating: "Xenopus represents a much more formidable predator than most anurans, which rely on the tongue for selective capture of rather small prey items. In Xenopus, prey capture employs a combination of toothed jaws that improve the grip on the prey, forelimbs that are used to fork the prey into the mouth, and the strong hindlimbs that can be used to rake the prey with the sharp claws. This shredding action enables Xenopus to tackle larger food items than could otherwise be ingested whole; indeed, groups of Xenopus may attack the same prey and can tear the body into fragments that can then be ingested. This method of feeding is particularly useful for scavenging."

Accounts of terrestrial prey in the stomachs of Xenopus species from Africa were often characterized as ambiguous, since their ability to forage out of water was undocumented (Noble, 1924; Inger and Marx, 1961; Tinsley, 1973; Tinsley et al., 1979; De Bruyn et al., 1996). Measey (1998b) recently has demonstrated that clawed frogs have the ability to capture prey out of the water and that feeding on terrestrial prey may indeed be a normal component of their foraging behavior. Nevertheless, aquatic prey predominate in all other diet studies.

In bodies of water where there are limited prey, adults will cannibalize young (Buxton, 1936; McCoid and Fritts, 1993; Picker, 1994). Larvae may act as collectors of nutrients such as seasonal single-celled algal blooms, which are unavailable to adults. Adults that cannibalize these larvae can thus rely indirectly on this phytoplankton food base (Savage, 1963; Picker, 1994; Tinsley et al., 1996). Cannibalism allows clawed frogs to colonize a body of water that does not offer a large prey base for the adults or to stay in a body of water that has been depleted of prey.

Although there has been much speculation about the possibility of predation on fishes, to date there have been no documented cases where clawed frogs have caused fish declines. Although not particularly adept at capturing actively swimming prey such as fish (Avila and Frye, 1978), clawed frogs have the capacity to find and eat fish eggs. Under confined conditions with unnaturally high densities of fish, such as occur in aquaculture, clawed frogs are indeed capable of consuming high numbers of fish (Branson, 1975; Hepher and Pruginin, 1981; Prinsloo et al., 1981; Schramm, 1986), but observations of fish predation have rarely been documented in nature in California (Lenaker, 1972; Zacuto, 1975; Lafferty and Page, 1997). Early accounts of fish in clawed frog stomachs may have been an artifact of collection methods (McCoid and Fritts, 1980b).

Lafferty and Page (1997) reported clawed frog predation on tidewater gobies (Eucyclogobiusnewberryi), a Federally Endangered species; tidewater gobies are sympatric with clawed frogs in Goleta Slough and Orange County estuaries (Swift et al., 1989). The Federally Endangered, unarmored threespine stickleback (Gasterosteusaculeatuswilliamsoni) is also sympatric with clawed frogs in the Santa Clara River (St. Amant, 1975). California's indigenous pupfish (Cyprinodon sp.) may be at particular risk from clawed frog introductions because their populations are confined, and clawed frogs can tolerate the chemical conditions and temperatures of the pupfish habitats.

The presence of high numbers of clawed frog larvae has been shown to directly impact Chinese silver carp (Hypothalmichthysmolitrix), which feed on phytoplankton and suspended detritus (Schramm, 1986). Based on food preferences, clawed frogs will likely compete with phytophagous and benthic feeding fish (Schoonbee et al., 1992).

O. Predators. Known predators of clawed frogs in Africa include members of many of the same taxa that consume native frogs in North America: invertebrates (Buxton, 1936), fish (Prinsloo et al., 1981), snakes (Sweeney, 1961), turtles (Rose, 1950), birds, and mammals (Worthington and Worthington, 1933; Loveridge, 1942; Rowe-Rowe, 1977). Even barnyard animals such as ducks and pigs are known to eat clawed frogs (Dreyer, 1913; Hey, 1949).

P. Anti-Predator Mechanisms. Harassed clawed frogs produce large amounts of an extremely slippery mucus from skin glands. Clawed frogs are purported to make dogs that attempt to eat them foam at the mouth in response to these skin secretions (Hey, 1949). Oral dyskinesia is produced in some North American and African water snakes when attempting to ingest clawed frogs (Barthalmus and Zielinski, 1988; Barthalmus, 1989; Zielinski and Barthalmus, 1989).

Surfacing behavior can become synchronized within a group of clawed frogs, apparently in response to the presence of potential predators (Baird, 1983).

R. Parasites. Clawed frogs are infected by a remarkably rich parasite fauna that includes over 25 genera from 7 major invertebrate groups (Tinsley, 1996). Most of the parasites probably do not persist in extralimital populations, due to a lack of suitable intermediate hosts. However, Lafferty and Page (1997) found African tapeworms (Cephalochlamysnamaquensis), ciliates (Nyctotherus sp.), and encysted larval nematodes in California populations. Other clawed frog populations sampled at four Southern California sites (n = 8, 39, 23, 30) exhibited tapeworm infestation levels of 100%, 92%, 91%, and 27%, respectively, with individual infestation levels ranging from 0–50 tapeworms (unpublished data). This tapeworm species has demonstrated an ability to infect other amphibians (Ranaangolensis, Dicroglossusoccipitalis, Pleurodelespoireti; Tinsley, 1996), which raises the possibility of parasite transmission to native fauna. An examination of a sample of clawed frogs from San Diego County (n = 21) revealed infections by an additional two species of protozoan ciliates (Balantidiumxenopodis and Protoopalinaxenopodus), a flagellate (Cryptobia sp.), and two monogeneans (Protopolystomaxenopodis and Gyrdycotylusgallieni), all of which are endemic in clawed frog populations in Africa (Kuperman et al., 2000).

4. Conservation. African clawed frogs are considered an invasive species and every reasonable attempt should be made to eradicate populations.

Acknowledgments. Many individuals provided intellectual stimulation, distribution information, field assistance, specimens, and data for this account, and I offer them my sincerest thanks: Patrick Davis, David Muth, Shawna Bautista, Jim Dole, Bill Taylor, Dennis Otsuka, Bobby Goodman, Mark Jennings, Ed Ervin, Robert Fisher, Karen Swaim, Dan Holland, Michael McCoid, Kevin Lafferty, Sam Sweet, and especially, Roger Hothem. For financial support while working on Edwards A.F.B., I am indebted to Wanda Deal and Mark Hagan of the Environmental Management Division of Edwards A.F.B., and the Davis Field Station of the Biological Resources Division, USGS.